Ineffectiveness of Over-the-Counter Total-Release Foggers Against the Bed Bug (Heteroptera: Cimicidae)

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HOUSEHOLD AND STRUCTURAL INSECTS

 Ineffectiveness of Over-the-Counter Total-Release Foggers Against the
                   Bed Bug (Heteroptera: Cimicidae)
                                       SUSAN C. JONES1     AND   JOSHUA L. BRYANT
           Department of Entomology, The Ohio State University, 2501 Carmack Road, Columbus, OH 43210-1065

                      J. Econ. Entomol. 105(3): 957Ð963 (2012); DOI: http://dx.doi.org/10.1603/EC12037
       ABSTRACT Field-collected bed bugs (Cimex lectularius L.) showed little, if any, adverse effects
       after 2-h direct exposure to the aerosolized pyrethroid(s) from three over-the-counter total-release
       foggers (Ôbug bombsÕ or ÔfoggersÕ); Hotshot Bedbug and Flea Fogger, Spectracide Bug Stop Indoor
       Fogger, and Eliminator Indoor Fogger. One Þeld-collected population, EPM, was an exception in that
       there was signiÞcant mortality at 5Ð7 d when bugs out in the open had been exposed to the Spectracide
       Fogger; mortality was low when these bugs had access to an optional harborage, a situation observed
       for all Þeld-collected populations when exposed to the three foggers. Even the Harlan strain, the
       long-term laboratory population that is susceptible to pyrethroids and that served as an internal control
       in these experiments, was unaffected if the bugs were covered by a thin cloth layer that provided
       harborage. In residences and other settings, the majority of bed bugs hide in protected sites where
       they will not be directly contracted by the insecticide mist from foggers. This study provides the Þrst
       scientiÞc data supporting the position that total-release foggers should not be recommended for
       control of bed bugs, because 1) many Þeld-collected bed bugs are resistant to pyrethroids, and they
       are not affected by brief exposure to low concentrations of pyrethrins and/or pyrethroids provided
       by foggers; and 2) there is minimal, if any, insecticide penetration into typical bed bug harborage sites.
       This study provides strong evidence that Hotshot Bedbug and Flea Fogger, Spectracide Bug Stop
       Indoor Fogger, and Eliminator Indoor Fogger were ineffective as bed bug control agents.

       KEY WORDS bug bomb, Cimex lectularius, fogger, pyrethroid, resistance

During the past decade, bed bugs (Cimex spp.) have               ease in which they are spread (Hwang et al. 2005, Eddy
become increasingly commonplace worldwide (Har-                  and Jones 2011).
lan et al. 2008). The bed bug, Cimex lectularius L., is             A dramatic increase in consumer products mar-
adapted for temperate climates and is the dominant               keted for bed bug control has accompanied the bed
species in the United States, whereas the tropical bed           bug resurgence. Over-the-counter (OTC) total-re-
bug, Cimex hemipterus (F.), is adapted for semitropical          lease foggers, commonly known as Ôbug bombsÕ or
to tropical climates (Usinger 1966). Bed bugs are tem-           Ôfoggers,Õ are marketed as consumer products for the
porary ectoparasites that feed exclusively on blood              control of many types of crawling and ßying house-
from humans and other warm-blooded animals. Bed                  hold insects. Decades ago, annual sales of foggers
bugs are recognized at the federal level as public               amounted to more than one per household (Green-
health pests (EPA 2002, CDC and EPA 2010). They are              berg 1963). The most recent estimate from the U.S.
largely nocturnal and spend most of their time hiding            Environmental Protection Agency (EPA) is that ⬇50
in cracks and crevices (Usinger 1966, Romero et al.              million foggers are used annually (http://epa.gov/
2010, Reis and Miller 2011).                                     oppfead1/cb/csb_page/updates/2010/new-foggers.
   Pyrethroid resistance is well documented and wide-            html). Foggers often are used by consumers as a low-
spread in Þeld-collected bed bugs and has been im-               cost alternative to professional pest control services;
plicated in the resurgence and challenge of bed bug              they typically are easy to use and require little effort.
control (Romero et al. 2007, Zhu et al. 2010, Bai et al.            Most foggers contain pyrethrins, pyrethroids, or
2011). Additionally, the re-emergence of bed bugs as             both, as active ingredients. Foggers act by broadcast-
human pests is associated with factors such as in-               ing an insecticide mist by way of an aerosol propellant.
creased international travel and commerce, changes in            The directions typically indicate that the can is to be
pesticide availability and pest management practices,            shaken well and positioned on a table or stand in the
and the publicÕs lack of awareness of bed bugs and the           center of the room then activated by depressing or
                                                                 removing a tab at the top center of the can; people and
                                                                 pets are to vacate the area during the treatment pe-
 1   Corresponding author, e-mail: jones.1800@osu.edu.           riod, usually 2 h. The canÕs contents are entirely de-

                                                          0022-0493/12/0957Ð0963$04.00/0 䉷 2012 Entomological Society of America
958                               JOURNAL OF ECONOMIC ENTOMOLOGY                                      Vol. 105, no. 3

pleted as aerosol insecticide droplets are rapidly re-      40 ⫾ 15% RH). In addition, the Harlan strain, which is
leased upwards into the airspace, where they remain         a pyrethroid-susceptible population (Zhu et al. 2010)
suspended then gradually settle onto exposed sur-           initially collected in 1973 from Ft. Dix, NJ, and labo-
faces.                                                      ratory reared thereafter with no known insecticide
   Foggers generally are not recommended for control        exposure, was used as an internal control. Each bed
of household pests because of concerns that 1) there        bug population was housed in a glass jar (13 cm high ⫻
is minimal insecticide penetration into pest harborage      7 cm dia; narrow-mouth Mason pint jar, Ball Corp.,
sites, which renders them ineffective as control agents;    BroomÞeld, CO) containing Þlter paper strips for har-
2) the broadcast insecticide application leaves pesti-      borage, with an organza fabric and Þlter paper cov-
cide residues on exposed surfaces and objects; and 3)       ering held in place with a screw-on metal ring.
the aerosol propellants may be highly ßammable, ca-            Bed bugs were reared in situ on a diet of warmed
pable of causing Þres and explosions (Potter 1999).         sodium-heparinized chicken blood using the He-
Foggers have been implicated in human injury and            motek 5W1 system (Discovery Workshops, Accring-
illnesses, often because of misuse of the products by       ton, England) with ParaÞlm as the membrane. Ap-
consumers. The U.S. Centers for Disease Control and         proximately every 7Ð14 d, each bed bug population
Prevention (CDC) reported a total of 466 cases of           was offered a bloodmeal until a majority of the bugs
acute, pesticide-related illness or injury associated       were replete.
with exposure to total-release foggers in eight states         Study Site. All experiments were conducted in three
between 2001 and 2006 (Wheeler et al. 2008). In terms       rooms in a vacant ofÞce building on the Ohio State
of the severity of these cases, 80% were classiÞed as       University campus, Columbus, OH. In each of the test
low, 18% were moderate, and 2% were high; health            rooms, 6 mil plastic sheeting (Blue Hawk, Grand Prai-
effects typically were temporary and most commonly          rie, TX) was installed to cover the drop ceiling, outlets,
involved the respiratory system. Additionally, the          and vents to prevent dispersion of the insecticide into
Washington State Department of Health classiÞed the         adjacent areas. The volume of the two treatment
death of a female infant as “suspicious,” because she       rooms was 32.5 m3 (1,190 ft3) and 35.0 m3 (1,280 ft3),
was found dead the morning after her apartment had          and the control room was 36.3 m3 (1,330 ft3).
been treated with three foggers. Another CDC report            Foggers. Three OTC indoor foggers, all obtained
highlighted illnesses associated with bed bug treat-        from a nationwide retailer, and all from United Indus-
ments in seven states between 2003 and 2010; one            tries Corp., St Louis, MO, were evaluated: Hotshot
fatality was associated with multiple factors including     Bedbug and Flea Fogger (0.05% pyrethrins, 0.1% es-
misuse of two fogger products (Jacobson et al. 2011).       fenvalerate, 0.1% piperonyl butoxide, 0.167% MGK
   The most common factors contributing to insecti-         264, 0.1% nylar) (Spectrum Group, St. Louis, MO),
cide exposure from foggers include inability or failure     Spectracide Bug Stop Indoor Fogger (0.1% tetrame-
to vacate before discharge of the fogger, unintentional     thrin, 0.6% cypermethrin) (Spectrum Group), and
fogger discharge, premature re-entry, excessive num-        Eliminator Indoor Fogger (0.515% cypermethrin)
ber of foggers, and failure to notify others nearby         (Chemisco, St. Louis, MO). A can of each fogger treats
(Wheeler et al. 2008). In an effort to minimize misuse      54.6 m3 (2,000 ft3) of unobstructed area. Only Hotshot
caused by failure to follow label instructions, EPA has     Fogger is speciÞcally labeled for use against bed bugs;
required manufacturers to make a number of labeling         the other two foggers are labeled for use against ßying
changes by 30 September 2011, to enhance clarity and        and crawling pests in homes. However, the latter two
draw increased attention to critical information (http://   products can be used against bed bugs in many states,
epa.gov/oppfead1/cb/csb_page/updates/2010/                  whose regulatory requirements are that only the site
new-foggers.html).                                          (e.g., indoors) has to be speciÞed by the label, not the
   The few available peer review publications regard-       particular pest.
ing the efÞcacy of foggers pertain to the German               Experimental Units. Test arenas consisted of petri
cockroach, Blattella germanica (L.), (Moore 1977,           dishes (100 ⫻ 15 mm; Fisherbrand, Pittsburgh, PA) or
Kardatzke et al. 1982, Ballard et al. 1984) and the cat     cylindrical plastic containers (50 ⫻ 37 mm; Pioneer
ßea, Ctenocephalides felis (Bouché) (Osbrink et al.        Plastics Inc., North Dixon, KY) whose sides had been
1986). There are no published data regarding the ef-        coated with Fluon (Insect-a-Slip Insect Barrier, Bio-
Þcacy of foggers against bed bugs. In this study, we        Quip Products, Rancho Dominguez, CA) to prevent
evaluated three foggers against recently Þeld-col-          bed bug escape. After arenas were provisioned with
lected populations of bed bugs as well as a long-term       bed bugs, replicates then were randomly distributed
laboratory strain to gain insights into the efÞcacy of      inside a 114-cm dia wading pool (General Foam Plastic
these OTC products.                                         Corp., Norfolk, VA) whose inner walls also had been
                                                            coated with Fluon. Two pools were prepared per room
                                                            so that two exposure conditions could be simultane-
                Materials and Methods
                                                            ously evaluated for each fogger or its control. A fogger
  Insects. Five bed bug populations (EPM, King,             can was positioned on a crate between the two pools
Kingry, Marcia, and Pointe) were collected between          such that it was ⬇30 cm above the ßoor and ⬇30 cm
July 2010 and March 2011 from residences in Colum-          from each pool edge. As speciÞed by the directions,
bus, OH, and they subsequently were maintained un-          the fogger was activated for a 2-h treatment period,
der ambient conditions in the laboratory (22 ⫾ 2⬚C,         then the room was opened and allowed to ventilate for
June 2012                   JONES AND BRYANT: INEFFECTIVENESS OF FOGGERS AGAINST BED BUGS                             959

   Fig. 1. Cumulative percentage corrected mortality (average ⫾ SE) at re-entry (30 min), 24 h, and 5Ð7 d for bed bugs
from six populations exposed to Hotshot Fogger in either an open petri dish or one containing a piece of paper that served
as an optional harborage (N ⫽ 10 replicates per mean [5 replicates consisting of 5 mixed-sex adults and 5 consisting of 5
mixed-stage nymphs]). Bars with different letters are signiÞcantly different based on TukeyÕs HSD test (P ⬍ 0.05).

30 min. A control room was similarly conÞgured but               Direct Exposure Versus Forced Harborage Experi-
without the fogger.                                           ments. Only the Hotshot Fogger was evaluated in
   The condition of bed bugs was assessed upon re-            these bioassays, and two test conditions were com-
entry (30 min) and then again at 24 h and 5Ð7 d. Bed          pared. In direct exposure tests, each cylindrical plastic
bugs were examined using a dissecting microscope as           container with bed bugs was kept uncovered; in forced
necessary. Each bugÕs condition was assessed based on         harborage tests, each container was covered with a
its behavioral response when probed:                          single layer of light-weight cotton broadcloth fabric
                                                              (Joann Fabrics, Columbus, OH) held in place by a
●   Healthy: The bed bug moves quickly and in a co-
                                                              rubber band. Two bed bug populations (EPM and
    ordinated manner to avoid stimulus.
                                                              Harlan) were exposed to the Hotshot Fogger; 10 rep-
●   Sluggish: reacts slowly, but makes coordinated
                                                              licates (5 consisting of 10 mixed-sex adults and 5 con-
    movements to avoid stimulus.
                                                              sisting of 10 mixed-stage nymphs) were established for
●   Ataxic: unable to coordinate movements to avoid
                                                              each of eight treatment combinations (2 popula-
    the stimulus. Ataxic bugs can right themselves after
                                                              tions ⫻ 2 harborage conditions ⫻ fogger and control).
    falling.
                                                              Hence, 800 bed bugs in total were used in this set of
●   Moribund: incapable of locomotion and exhibiting
                                                              bioassays.
    movement only of appendages or other body parts.
                                                                 Data Analysis. The numbers of moribund plus dead
●   Dead: no movement whatsoever.
                                                              bed bugs were pooled for analysis of bed bug mortal-
   Direct Exposure Versus Optional Harborage Experi-          ity. Treatment data were corrected for control mor-
ments. All three foggers were evaluated against bed           tality using AbbotÕs formula (Abbott 1925). Adults and
bugs in these bioassays. Bed bugs were either directly        nymphs were combined for analysis. Data were sub-
exposed in open, unprovisioned petri dishes, or they          jected to a repeated-measures analysis of variance
were placed in petri dishes provisioned with a 80 mm          (ANOVA) using Statistica 6.1 (StatSoft Inc. 2002),
dia Þlter paper disc (Whatman no. 1, Whatman Inter-           with observation time as the repeated-measures factor
national Ltd., Maidstone, England) that bed bugs              and population and harborage as categorical predictor
could hide underneath (optional harborage). The               variables. TukeyÕs honestly signiÞcant difference
Hotshot Fogger was evaluated against all six popula-          (HSD) test was used for post hoc comparison of means
tions of bed bugs, and both the Spectracide Fogger and        for signiÞcant main effects and interaction effects.
Eliminator Fogger were evaluated against three bed            When overall mean control mortality at an observa-
bug populations (EPM, Marcia, and Harlan). For the            tion time exceeded 15%, all data for that observation
Hotshot Fogger, 10 replicates, 5 consisting of 5 mixed-       were considered unreliable and were not analyzed.
sex adults and 5 consisting of 5 mixed-stage nymphs,
were established for each of 24 treatments: 6 bed bug
                                                                                        Results
populations ⫻ 2 harborage conditions ⫻ 2 treatments
(fogger and control). Hence, a total of 1,200 bed bugs          Hotshot Fogger. Optional Harborage. All Þve Þeld-
was used in this set of bioassays to evaluate the Hot-        collected bed bug populations showed little, if any,
shot Fogger. For both the Spectracide Fogger and the          adverse effects after 2 h of direct exposure to aero-
Eliminator Fogger, 10 replicates were similarly estab-        solized pyrethroids from the Hotshot Fogger (Fig. 1).
lished for each of 12 treatment combinations (3 pop-          SigniÞcantly high mortality was observed consistently
ulations ⫻ 2 harborage conditions ⫻ fogger and con-           only for the Harlan strain, the long-term laboratory
trol), providing a total of 600 bed bugs per product.         population that is susceptible to pyrethroids and that
960                                  JOURNAL OF ECONOMIC ENTOMOLOGY                                             Vol. 105, no. 3

                                                                  tality was evident at re-entry, but when they were
                                                                  provided an optional harborage, mortality was time
                                                                  dependent, with 62% mortality at re-entry, 78% at 24 h,
                                                                  and 100% at 5Ð7 d. In all other treatment and control
                                                                  groups, mortality averaged 2.1% and was nonsigniÞ-
                                                                  cant, with two exceptions (at 5Ð7d, Pointe bugs with-
                                                                  out a harborage exhibited 28% mortality after expo-
                                                                  sure to the fogger and Harlan control bugs without a
                                                                  harborage had 24% mortality).
                                                                     Forced Harborage. Figure 2 shows that the Þeld-
                                                                  collected EPM population was unaffected by the Hot-
                                                                  shot Fogger regardless of whether bugs were directly
                                                                  exposed or inside a harborage, but more importantly,
                                                                  the susceptible Harlan strain was unaffected if the
   Fig. 2. Cumulative percentage corrected mortality (av-         bugs were covered by a thin cloth layer that provided
erage ⫾ SE) at re-entry and 24 h for bed bugs from two            harborage. The main effects of population (F ⫽ 156.34;
populations exposed to Hotshot Fogger either in an open
container or in a forced harborage wherein each container
                                                                  df ⫽ 1, 36; P ⬍ 0.001) and harborage (F ⫽ 166.66; df ⫽
was covered with thin cotton fabric (N ⫽ 10 replicates per        1, 364; P ⬍ 0.001) were signiÞcant, but observation
mean [5 replicates consisting of 10 mixed-sex adults and 5        time (re-entry and 24 h) (F ⫽ 0.36; df ⫽ 1, 36; P ⫽ 0.55)
consisting of 10 mixed-stage nymphs]). Bars with different        was not. Because of high control mortality (16.5%),
letters are signiÞcantly different based on TukeyÕs HSD test      data for the 5Ð7 d observation were excluded from
(P ⬍ 0.05).                                                       analysis. The two-way interaction, population ⫻ har-
                                                                  borage, was signiÞcant (F ⫽ 157.83; df ⫽ 1, 36; P ⬍
served as an internal control in these experiments.               0.001) because only Harlan bugs exposed to the Hot-
When Harlan bed bugs were directly exposed in open                shot Fogger without a harborage experienced signif-
containers, all bugs were moribund or dead at re-                 icantly higher average mortality (97%) than controls
entry, but when this population was provided an op-               (2.4%) and the EPM bugs (7.5%).
tional harborage, mortality was signiÞcantly lower at                Spectracide Fogger. Optional Harborage. When ex-
re-entry but progressed over time (Fig. 1).                       posed to the Spectracide Fogger, the mortality trend
   Population (F ⫽ 625.31; df ⫽ 5, 108; P ⬍ 0.001),               among populations was Harlan ⬎ EPM ⬎ Marcia (Fig.
harborage (F ⫽ 28.38; df ⫽ 1, 108; P ⬍ 0.001), and                3). The main effects of population (F ⫽ 307.2; df ⫽ 2,
observation time (F ⫽ 22.23; df ⫽ 2, 216; P ⬍ 0.001)              54, P ⬍ 0.001), harborage (F ⫽ 13.72; df ⫽ 1, 54; P ⬍
were signiÞcant main effects. The full interaction ef-            0.001), and observation time (F ⫽ 30.10; df ⫽ 2, 108;
fect (population ⫻ harborage ⫻ observation time)                  P ⬍ 0.001) were signiÞcant (Fig. 3).
was signiÞcant (F ⫽ 8.19; df ⫽ 10, 216; P ⬍ 0.001)                   The three-way interaction of population ⫻ harbor-
primarily because of high, but variable, mortality in             age ⫻ observation (F ⫽ 11.15; df ⫽ 4, 108; P ⬍ 0.001)
the susceptible Harlan strain (Fig. 1); Þeld-collected            was signiÞcant, because at re-entry, Harlan bed bugs
bed bug strains typically exhibited low mortality re-             experienced signiÞcantly higher mortality in open
gardless of observation time. When Harlan bed bugs                dishes (100%) than when they had access to a har-
were directly exposed in open containers, 100% mor-               borage (69%); mean mortality further increased to

   Fig. 3. Cumulative percentage corrected mortality (average ⫾ SE) of bed bugs from three populations exposed to
Spectracide Fogger in either an open petri dish or one containing a piece of paper that served as an optional harborage when
observed at re-entry, 24 h, and 5Ð7 d (N ⫽ 10 replicates per mean [5 replicates consisting of 5 mixed-sex adults and 5 consisting
of 5 mixed-stage nymphs]). Bars with different letters are signiÞcantly different based on TukeyÕs HSD test (P ⬍ 0.05).
June 2012                 JONES AND BRYANT: INEFFECTIVENESS OF FOGGERS AGAINST BED BUGS                          961

91% at 24 h and to 98% at 5Ð7 d. Additionally, EPM bugs    mero et al. 2007, Zhu et al. 2010, Bai et al. 2011), it is
in open dishes had a signiÞcant increase in mortality      likely that pyrethrin- and pyrethroid-based foggers
from 0% (re-entry) to 24% (24 h) to 66% (5Ð7 d).           will have little, if any, impact on modern-day bed bug
However, when EPM bugs had access to a harborage,          infestations. Note also that Hotshot Fogger was inef-
their mortality was very low, equivalent to controls.      fective against Þeld-collected bed bugs despite the
   Eliminator Fogger. Optional Harborage. In bioas-        presence of piperonyl butoxide, an insecticide syner-
says with the Eliminator Fogger, the paper harborage       gist that has been shown to somewhat improve prod-
curled, resulting in partial or complete escape of bed     uct efÞcacy in pyrethroid-resistant bed bugs (Romero
bugs in some replicates, and thus harborage could not      et al. 2009a).
be evaluated as a main effect. Additionally, control          A very important Þnding was that a forced harbor-
mortality at 5Ð7 d was quite high (37.8%); hence, this     age negated any fogger effects on the susceptible Har-
observation time was omitted from analysis.                lan strain (Fig. 2). Furthermore, having access to a
   Bed bugs from two Þeld-collected populations,           paper harborage resulted in delayed mortality in py-
EPM and Marcia, exhibited no signiÞcant adverse ef-        rethroid-susceptible Harlan bugs (Figs. 1 and 3) and
fects at re-entry and 24 h after being exposed in open     signiÞcantly reduced mortality for EPM bugs exposed
containers to the Eliminator Fogger. Overall mortality     to Spectracide (Fig. 3). Hence, our research supports
was quite low for controls (6%) as well as for Marcia      the view that total-release foggers lack the ability to
(8%) and EPM (3%) exposed to the fogger. SigniÞ-           penetrate into typical harborages used by many
cantly high mortality was observed only for the sus-       household insects, therefore rendering these products
ceptible Harlan strain. The main effect of population      ineffective as control agents. Our Þndings provide
(F ⫽ 564.5; df ⫽ 2, 27; P ⬍ 0.001) was signiÞcant and      support for OsbrinkÕs et al. (1986) suggestion that
affected bed bug mortality whereas observation time        reduced mortality of cat ßeas on disks of carpet versus
did not (re-entry and 24 h) (F ⫽ 1.7; df ⫽ 1, 27; P ⫽      Þlter paper was likely because of the carpet providing
0.2). The population ⫻ observation interaction was         a refuge for cat ßeas to avoid the mist from foggers.
signiÞcant (F ⫽ 7.2; df ⫽ 2, 27; P ⫽ 0.003) because           In residences and other settings, the majority of bed
Marcia mortality was signiÞcantly lower at re-entry        bugs hide in protected sites during photophase. Reis
(2%) than at 24 h (14%) whereas EPM was similar at         and Miller (2011) observed that ⱖ80% of bed bugs
re-entry (2%) and 24 h (8%). In contrast, the long-        remain in harborages during the day regardless of their
term laboratory population, Harlan, had consistently       feeding status. They found that unfed, rather than fed,
high mortality at re-entry (100%) and 24 h (100%).         bed bugs leave their harborages at night to search for
                                                           a bloodmeal. It could be suggested that setting off
                                                           foggers during nighttime rather than day, perhaps,
                      Discussion
                                                           would impact more bed bugs (e.g., hungry bugs
   Field-collected bed bugs typically were not affected    searching for a host), but there would be no host cues
by direct exposure for 2 h to the aerosolized pyre-        to stimulate searching behavior because the area has
throid(s) emanating from any of the three total-re-        to be vacated when the fogger is activated. The innate
lease foggers (Figs. 1Ð3), with the exception of EPM,      behavior of bed bugs to remain in tight, inaccessible
which experienced signiÞcantly high mortality at 5Ð7       harborages for a prolonged period of time has impor-
d when bugs out in the open had been exposed to the        tant implications for fogger efÞcacy against bed bug
Spectracide Fogger but not when these bugs had ac-         populations. Because of bed bugsÕ propensity for hid-
cess to a harborage (Fig. 3). In contrast, the Harlan      ing sites, the majority of the population will not be
strain, the long-term laboratory population that is sus-   directly contracted by the insecticide mist from total-
ceptible to pyrethroids, experienced signiÞcantly high     release foggers, hence rendering these products inef-
mortality when directly exposed to any of the three        fective.
foggers (Figs. 1Ð3). Hence, pyrethroid resistance ap-         Another serious concern is that fogging can actually
pears to play a role in the foggersÕ failure to kill bed   acerbate problems with some insects. For example,
bugs.                                                      German cockroaches prematurely released their ooth-
   Subsequent genotyping of bed bugs used in our           ecae, resulting in an increase in newly hatched
study indicated that all Þve Þeld-collected populations    nymphs, in response to fogging with pyrethrins (Kar-
possessed both known kdr mutations for pyrethroid          datzke et al. 1982) or dichlorvos (Ballard et al. 1984).
resistance, V419L and L925I (A.T.H., S.C.J., J.L.B., and   Furthermore, German cockroaches moved from
O. M. unpublished data), but the Harlan strain pos-        fogged units to adjacent units in 50% of apartments,
sessed none, which is in agreement with the Þndings        with increased catches of cockroaches the night after
of Zhu et al. (2010). The dual compliment of kdr           the fogger treatment (Ballard et al. 1984). In fact,
mutations is the most commonly encountered bed bug         pyrethroids, the active ingredients of foggers tested
haplotype in Ohio (A.T.H., S.C.J., J.L.B., and O. M.       here, have been shown to increase locomotor activity
unpublished data), and it appears to be very prevalent     of bed bugs upon contact with dry deposits (Romero
in Ohio as well as throughout much of the United           et al. 2009b). This potential behavioral effect of fog-
States (Zhu et al. 2010). Furthermore, it is highly        gers on bed bugs needs to be evaluated as it may
unlikely that any Þeld population would be as suscep-      increase the difÞculties associated with bed bug con-
tible as the Harlan strain. Because resistance is wide-    trol. Bed bugs are notoriously difÞcult to control in
spread in Þeld-collected bed bug populations (Ro-          multi-unit buildings (Wang et al. 2009, Harlan et al.
962                                 JOURNAL OF ECONOMIC ENTOMOLOGY                                           Vol. 105, no. 3

2008, Eddy and Jones 2011), and any product that                   lectularius). PLoS One 6: e16336. (doi: 10.1371/journal.
further disperses the bed bugs to adjacent units is of             pone.0016336).
grave concern.                                                  Ballard, J. B., R. E. Gold, and J. D. Rauscher. 1984. Effec-
   All three total-release foggers claim “kills on con-            tiveness of six insecticide treatment strategies in the re-
tact” yet all Þeld-collected bed bugs were unaffected              duction of German cockroach (Orthoptera: Blattellidae)
upon re-entry. Furthermore, 5Ð7 d later, most of these             populations in infested apartments. J. Econ. Entomol. 77:
                                                                   1092Ð1094.
bugs remained unaffected, which suggests that these
                                                                (CDC and EPA) Centers for Disease Control and Preven-
pyrethroid-based foggers lack delayed toxicity and                 tion & U.S. Environmental Protection Agency. 2010.
have no long-term residual efÞcacy against Þeld pop-               Joint statement on bed bug control in the United States from
ulations of bed bugs (Figs. 1 and 3).                              the U.S. Centers for Disease Control and Prevention (CDC)
   The public is ill-served when products do not per-              and the U.S. Environmental Protection Agency (EPA).
form in accordance with labeling and use directions                (http://www.cdc.gov/nceh/ehs/Docs/Joint_Statement_
claims. The use of ineffective insecticide products                on_Bed_Bug_Control_in_the_US.pdf).
means that people are wasting money, and they are               Eddy, C., and S. C. Jones. 2011. Bed bugs, public health, and
delaying effective treatment of insect pests whose                 social justice: part 1, a call to action. J. Env. Health 73:
populations are ever increasing in their residence and             8 Ð14.
likely spreading to others. Furthermore, insecticides           (EPA) U.S. Environmental Protection Agency. 2002. No-
are unnecessarily being introduced into the environ-               tice to manufactures, formulators, producers, regis-
                                                                   trants, and applicators of pesticide products (Pesticide
ment, and people (and insects) are being exposed to
                                                                   Registration Notice 2002-1). (http://www.epa.gov/PR_
insecticide residues, while further reinforcing insec-             Notices/pr2002-1.pdf).
ticide resistance in insects. Despite the widespread            Greenberg, D. S. 1963. Pesticides: White House advisory
use of OTC foggers, there is only limited research on              body issues report recommending steps to reduce hazard
these products, and the data suggest that pyrethrin-               to public. Science 140: 878 Ð 879.
and pyrethroid-based foggers are ineffective against            Harlan, H. J., M. K. Faulde, and G. J. Baumann. 2008. Bed-
diverse household insect pests. For example, Osbrink               bugs, pp. 131Ð153. In X. Bonnefoy, H. Kampen, and K.
et al. (1986) found that foggers containing 0.5% py-               Sweeney (eds.), Public health signiÞcance of urban pests.
rethrins failed to control cat ßeas, but those containing          World Health Organization Regional OfÞce for Europe,
an insect growth regulator (IGR) provided ßea con-                 Copenhagen, Denmark.
trol for up to 60 d. Moore (1977) found that the least          Hwang, S. W., T. J. Svoboda, I. J. De Jong, K. J. Kabasele, and
effective total-release aerosols for German cockroach              E. Gogosis. 2005. Bed bug infestations in an urban en-
                                                                   vironment. Emerg. Infect. Dis. 11: 533Ð538.
control were 0.25% resmethrin-tetramethrin.
                                                                Jacobson, J. B., K. Wheeler, R. Hoffman, Y. Mitchell, J. Beck-
   In conclusion, our study provides strong evidence               man, L. Mehler, P. Mulay, A. Schwartz, R. Langley, B.
that Hotshot Bedbug and Flea Fogger, Spectracide                   Diebolt-Brown, et al. 2011. Acute illnesses associated
Bug Stop Indoor Fogger, and Eliminator Indoor Fog-                 with insecticides used to control bed bugsÑseven states,
ger were ineffective as bed bug control agents. The                2003Ð2010. Morib. Mortal. Wkly. Rep. 60: 1269 Ð1274.
low concentrations of pyrethrins, pyrethroids, or both,         Kardatzke, J. T., D. P. Driggers, and J. H. Nelson. 1982.
and the brief exposure provided by these total-release             Cockroach control. Pest Control 50: 53: 56.
foggers had little impact on modern-day bed bugs. Our           Moore, R. C. 1977. Field tests of pyrethrins and resmethrin
data also support the position that currently marketed             applied with ULV generators or total release aerosols to
total-release foggers should not be recommended for                control the German cockroach. J. Econ. Entomol. 70:
treating bed bug infestations because these products               86 Ð 88.
provide no residual and they allow for minimal, if any,         Osbrink, W.L.A., M. K. Rust, and D. A. Reierson. 1986. Dis-
                                                                   tribution and control of cat ßeas in homes in southern
insecticide penetration into typical bed bug harborage
                                                                   California (Siphonaptera: Pulicidae). J. Econ. Entomol.
sites.                                                             79: 135Ð140.
                                                                Potter, M. F. 1999. Limitations of home insect foggers (Ôbug
                                                                   bombsÕ). (http://www.ca.uky.edu/entomology/entfacts/
                   Acknowledgments                                 entfactpdf/ef643.pdf).
                                                                Reis, M. D., and D. M. Miller. 2011. Host searching and
   We thank Andrew Hoelmer, Mark Janowiecki, and
Thomas Peterson for their assistance with this study. We also      aggregation activity of recently fed and unfed bed bugs
gratefully acknowledge Harold HarlanÕs contribution of pes-        (Cimex lectularius L.). Insects 2: 186 Ð194.
ticide-susceptible bed bugs. We appreciate Dave ShetlarÕs       Romero, A., M. F. Potter, and K. F. Haynes. 2009a. Evalu-
review of the manuscript. This research was supported in part      ation of piperonyl butoxide as a deltamethrin synergist for
by State and Federal funds appropriated to the Ohio Agri-          pyrethroid-resistant bed bugs. J. Econ. Entomol. 102:
cultural Research and Development Center, The Ohio State           2310 Ð2315.
University.                                                     Romero, A., M. F. Potter, and K. F. Haynes. 2009b. Behav-
                                                                   ioral responses of the bed bug to insecticide residues.
                                                                   J. Med. Entomol. 46: 51Ð57.
                                                                Romero, A., M. F. Potter, and K. F. Haynes. 2010. Circadian
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